Can the environment have a genetic basis? a case study of seedling establishment in Arabidopsis thaliana

The timing of seed germination determines the environment experienced by a plant’s most vulnerable life stage—the seedling. Germination is environmentally cued, and genotypes can differ in their sensitivity to environmental cues. When genotypes differ in their response to cues, and when cues accurately predict the post-germination environment, the post-germination environment experienced by seedlings can itself have a genetic basis and potential to evolve. We tested for genetic differences in the post-germination environment using Arabidopsis thaliana genotypes that vary in seed dormancy, a trait known to alter germination time. We dispersed seeds into the field in five seasonal cohorts over 1.5 years, observed germination timing for 5297 individuals, and measured the soil temperature and moisture experienced by individuals throughout their life cycle. We found that genotypes differed in the environments they experienced during seedling establishment. This environmental variation occurred because genotypes differed in their environmental sensitivity to germination cues, and pre-germination cues were correlated with post-germination environments. Seeds exhibited temporal habitat selection by germinating into a non-random subset of environmental conditions available, and seed dormancy increased the consistency of habitat selection. Strikingly, the post-germination environment affected fitness by altering the probability of seedling survival, such that genotypes that engaged in stronger habitat selection were less likely to reach reproduction. Our results suggest that environmentally-cued development may be a widespread mechanism by which genotypes can differ in the environment they experience, introducing the possibility that the environment itself can be inherited and can evolve.